Effects of Seasonal Conditions on Abundance of Malaria Vector Anopheles stephensi Mosquitoes, Djibouti, 2018–2021

We describe the influence of seasonal meteorologic variations and rainfall events on Anopheles stephensi mosquito populations during a 40-month surveillance study at a US military base in Djibouti. Focusing surveillance and risk mitigation for An. stephensi mosquitoes when climatic conditions are optimal presents an opportunity for malaria prevention and control in eastern Africa.

We describe the influence of seasonal meteorologic variations and rainfall events on Anopheles stephensi mosquito populations during a 40-month surveillance study at a US military base in Djibouti. Focusing surveillance and risk mitigation for An. stephensi mosquitoes when climatic conditions are optimal presents an opportunity for malaria prevention and control in eastern Africa.
We used the Shapiro-Wilk test to check normal distribution of An. stephensi mosquito data and Pearson correlation coefficient to evaluate relationships between mosquito abundance and climatic variables. We categorized temperatures as either above or equal to or below median annual temperature (30°C). We  grouped rainfall data according to frequency at each of 5 levels: 0, 0.2-4.9, 5-21, 21.1-39.9, and 40-155 mm/ week. We used Poisson regression for univariate and multivariate analyses to determine associations between mosquito abundance and predictor variables, and used PROC GENMOD in SAS version 9.4 (SAS Institute, Inc., https://www.sas.com) to perform logistic regression. We expressed results in incidence rate ratios (IRR) and used p = 0.05 as the cutoff for statistical significance.
An. stephensi represented 95.6% of all Anopheles spp. mosquitoes we identified. Using dataset B to compare effectiveness of trap types, we found that MM traps captured 25.6% more An. stephensi mosquitoes than did CDC traps (IRR 2.3; p<0.0001) (Appendix Table, Figure). Univariate regression analysis of datasets A and B (Appendix Table) demonstrated that An. stephensi mosquito populations persisted year-round. Related to seasonal distribution, in dataset A, winter accounted for 56.4% of Anopheles spp. mosquito captures; spring, 28.1%; fall, 9.8%; and summer, 5.7%. In dataset B, winter accounted for 55.2% of An. stephensi mosquito captures; spring, 37.1%; fall, 6.9%; and summer, 0.8%. Associations between An. stephensi mosquito abundance and monthly mean temperatures ( Figure 1) were positive for temperatures <30 (IRR 5.5 for dataset A, 7.4 for dataset B; p<0.0001). In dataset A, 85% of Anopheles spp. mosquitoes were collected at temperatures ≤30°C; for dataset B, the percentage was 94% of An. stephensi mosquitoes (Appendix Table).

Conclusions
We speculate that the slow continuous release of CO 2 of MM traps contributed to higher captures of An. stephensi mosquitoes than for CDC traps. In a study in Malaysia, MM traps performed 3-fold better than CDC traps for capturing Anopheles spp. mosquitoes (12), demonstrating the suitability of MM traps for An. stephensi mosquito surveillance in urban settings and areas with limited or no access to dry ice (13).
An. stephensi mosquitoes were present yearround but at substantially higher populations during winter (mean temperature 26°C, average rainfall 2.3 mm/week) and spring (mean temperature 29°C, average rainfall 7.3 mm/week). A previous study observed a similar link between temperature and An. stephensi mosquito populations, with 29°C assessed as optimal (14). We linked the bionomics of An. stephensi mosquito abundance in urban areas to human-modified conditions, such as air conditioningproduced condensation, water storage tanks, open jerry cans, and water-filled tires following rainfall, all of which increased favorable mosquito habitats (1) and in which we observed larval habitats around CLDJ. Flash flooding in Djibouti did not increase An. stephensi mosquito abundance. In fact, flooding might have destroyed laid eggs, hatched larvae, and temporary larval habitats, as was reported in China (15), possibly explaining higher population growth after periods of rainfall of 21.1-39.9 mm/week than 40-155 mm/week. Because breeding sites in urban areas depend as much on human-generated water sources as rainfall, adult mosquitoes were able to persist even during periods of low precipitation (14). We found that periods of rainfall at 21.1-39.9 mm/ week and temperatures slightly <30°C were optimal for adult An. stephensi mosquito abundance. Therefore, surveillance and control efforts should be most intense during times of the year when these conditions are common. However, because An. stephensi mosquitoes are present year-round, prevention and control measures cannot be relaxed during any season (Appendix).
Although our study was set at CLDJ facilities, conditions were comparable to other urban settings in Djibouti, which should encourage local health authorities to benefit from our data. The persistence of mosquito populations at CLDJ, which regularly monitors and employs control efforts, should raise the alarm for increased malaria risk in densely populated city areas with fewer public health and disease control resources. Given limited resources, we recommend targeted reduction of An. stephensi larval habitat in this area.